B-Cell Epigenetic Modulation of IgA Response by 5-Azacytidine and IgA Nephropathy.

Yu, Shanshan; Li, Xiang; Wang, Ting; Li, Jingyi; Li, Hongzhi; Xu, Ying; Hu, Yanling; Zhu, Fubin et al. · J Am Soc Nephrol · 2024

basic_science · Level V

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Abstract

Dysregulated IgA production plays a key role in the pathogenesis of IgA nephropathy. Increased 5-methylcytosine modification, an epigenetic regulatory mechanism, exaggerated IgA nephropathy phenotype in mice. Conversely, inhibition of 5-methylcytosine modification ameliorated progression of IgA nephropathy–like kidney disease in mice. IgA nephropathy is an important global cause of kidney failure. Dysregulation of IgA production is believed to play a key role in IgA nephropathy pathogenesis; however, little is known about the epigenetic mechanisms, such as RNA 5-methylcytosine (5mC) modification, in regulating IgA synthesis. To decipher the role of RNA 5mC in regulation of IgA class switch, the microRNA (miR)-23b<sup>−/−</sup> and <i>Lactobacillus casei</i> (Chinese Industrial Microbial Culture Collection Center) cell wall extract–induced Kawasaki disease mice were treated with 5-azacytidine. <i>Trdmt1</i><sup>−/−</sup> and double <i>Trdmt1</i><sup>−/−</sup>/<i>miR-23b</i><sup>−/−</sup> mice and <i>Aid</i><sup>−/−</sup> mice or <i>Aid</i><sup>−/−</sup>/<i>miR-23b</i><sup>−/−</sup> mice were also used. We showed that <i>miR-23b</i> downregulated expression of Transfer RNA Aspartic Acid Methyltransferase 1 and consequently reduced 5mC (m<sup>5</sup>C) RNA modification and IgA synthesis in B cells. Inhibition of m<sup>5</sup>C RNA modification normalized serum IgA levels and ameliorated progression of the IgA nephropathy–like kidney disease in <i>miR-23b</i><sup>−/−</sup> and Kawasaki disease mice, while mesangial IgA and C3 deposition failed to develop in <i>Trdmt1</i><sup>−/−</sup> <i>miR-23b</i><sup>−/−</sup> mice. By contrast, increased m<sup>5</sup>C RNA modification resulted in an exaggerated IgA nephropathy phenotype. <i>miR-23b</i> regulation of serum IgA levels and the development of an IgA nephropathy–like kidney disease in <i>miR-23b</i><sup>−/−</sup> and Kawasaki disease mice is likely mediated through TRDMT1-driven 5mC RNA modification in B cells, resulting in impaired activation-induced cytidine deaminase activity and IgA class switch recombination. This study revealed TRDMT1-induced RNA 5mC methylation regulated IgA class switch, and inhibition of RNA 5mC by 5-azacytidine ameliorated progression of IgA nephropathy.